PRIMARY RESEARCH PAPER

Spatial pattern of hydrolittoral rock encrusting assemblagesalong the salinity gradient of the Baltic Sea

Monika Grabowska . Piotr Kuklinski

Received: 24 June 2014 / Revised: 3 July 2015 / Accepted: 25 July 2015 / Published online: 8 August 2015

� Springer International Publishing Switzerland 2015

Abstract This study compared the diversity param-

eters and structures of encrusting assemblages in two

habitats situated at two levels of shallow rocky shore:

hydrolittoral and littoral along the Baltic Sea system.

We investigated the variability and level of distinc-

tiveness of the hydrolittoral encrusting fauna based on

species biodiversity and distribution, and compared

these featureswith those of communities inhabiting the

adjacent shallow littoral zone (3-m depth). Structural

similarities and differences between the encrusting

assemblages from adjacent hydrolittoral and littoral

zones were studied within 14 locations distributed

along the northern coastline of the Baltic Sea. Multi-

variate analysis indicates that salinity had the greatest

influence on the structure of the investigated assem-

blages.Most of the observed hydrolittoral assemblages

contained the same species as the littoral zone. This

result indicated a shared common species pool with

similar large-scale patterns of species distributions

with some variability in the dominating species

between zones. The similarity between species

composition of the hydrolittoral and littoral assemblages

decreased with increase of salinity. Additionally, with

higher species richness and the occurrence of marine

specialists adapted to hydrolittoral conditions, the role of

the rock size in the frequency of species occurrence and

assemblage diversity was less significant.

Keywords Rocky coast � Encrusting assemblages �Fauna � Environmental gradients � Baltic Sea

Introduction

Coastal marine communities are affected by a variety

of physical, chemical and biological disturbances (e.g.

Bonsdorf & Pearson, 1999; Hanninen & Vuorinen,

2001; Eriksson & Bergstrom, 2005; Rousi et al., 2011)

that modify recruitment conditions, influence species

richness, diversity and distribution (Bonsdorff, 2006;

Haanes & Gulliksen, 2011).

In marginal marine habitats, such as the intertidal

zone, stress is considered to be a structuring factor for

benthic community zonation, especially for those

sessile organisms sensitive to disturbances (Olenin,

1997; Araujo et al., 2012). Intensified coastal distur-

bance is associated with tidal basins, particularly

where factors such as increased wave action, sea level

changes or, in some areas, winter ice formation are

observed (Barnes & Arnold, 1999; Araujo et al.,

2012). Assemblages of marine organisms in these

areas are more susceptible to difficult conditions

Handling editor: Jonne Kotta

M. Grabowska (&) � P. KuklinskiInstitute of Oceanology Polish Academy of Sciences,

Sopot, Poland

e-mail: monikao@iopan.gda.pl

P. Kuklinski

Natural History Museum, Cromwell Road,

London SW7 5BD, UK

123

Hydrobiologia (2016) 765:297–315

DOI 10.1007/s10750-015-2421-z

resulting from increased sedimentation, overturning or

scouring (Therriault & Kolasa, 2000; Heaven &

Scrosati, 2008). Populations at the boundary of their

occurrence, for example those inhabiting the seashore,

are typically smaller (Raffaelli & Hawkins, 1996; Guo

et al., 2005) and are characterized by a lower

abundance compared with populations located deeper

in the sea (Sagarin et al., 2006).

Although the Baltic Sea is considered to be a non-

tidal basin, seasonal and daily sea level variability can

be significant and, over shorter time scales, the sea is

affected by meteorological forcing (Johansson et al.,

2001; Zaitseva-Parnaste et al., 2009). These condi-

tions can affect supralittoral or ‘hydrolittoral’ zone

(the latter term being used in this study). As a result of

significant hydrodynamic effects, the abiotic and

biotic features of this zone are particularly vulnerable

to physical disturbance from the constant water

mixing (Schumann et al., 2006). Position along the

land–sea gradient can directly influence physical and

biological processes across the water column, mainly

by controlling their intensity and thus influencing

community composition (Terlizzi et al., 2007).

The hydrolittoral zone is regularly or occasionally

exposed by the action of wind and is separated from

littoral habitats below the high water mark (Davies

et al., 2004). The hydrolittoral zone of the Baltic Sea

constitutes the uppermost part of the submarine

coastal slope and is adjacent to the species-rich littoral

zone (Olenin, 1997). This area is a very dynamic

environment (in terms of waves and currents) and is

affected by seasonal temperature and salinity fluctu-

ations (Olenin, 1997). The results from previous

studies investigating littoral communities in brackish

water bodies suggest that the salinity is a key

determinant of community structure and species

distribution over the large scale (Bonsdorf & Pearson,

1999; Cognetti & Maltagliati, 2000; Schernewski &

Wielgat, 2004; Zetler et al., 2007) and it has been

suggested that this is a result of differential tolerances

of different species to salinity conditions (Westerbom

et al., 2002; Johannesson & Andre, 2006; Khlebovich

& Aladin, 2010). Recent studies investigating the

distribution of fauna along the gradient of increasing

salinity in the Baltic Sea have shown that the

assemblage is transformed from dominated by a few

opportunistic species adapted to brackish waters, to

communities with a higher number of rare species in

the higher salinity North Sea (Telesh et al., 2013).

In this study, we investigate small- and large-scale

variability in the structure of encrusting faunal

assemblages in the shallow rocky coast of the Baltic

Sea. Encrusting fauna is defined here as all sessile

animals attached to the sampled rocks. The results of

previous studies suggest that the effect of low salinity

[leading to a lower number of species, as found in the

brackish water littoral zone (see Zettler et al., 2014)],

would have a similar effect on hydrolittoral encrusting

assemblages. We hypothesize that the large-scale

spatial pattern of the structure of hydrolittoral encrust-

ing assemblages (measured in terms of species com-

position, number and abundance) along the salinity

gradient would be similar to large-scale distribution

trends found for other Baltic Sea ecological forma-

tions (e.g. Bonsdorff, 2006, Telesh et al., 2013).

In temperate fully marine seas, intertidal commu-

nities differ substantially from those found in the

deeper subtidal range, often containing species that are

specialists adapted to the intertidal zone only (Raf-

faelli & Hawkins, 1996). In contrast, it has been

observed that in regions described as more disturbed,

including polar areas, the intertidal community often

resembles that of the nearby subtidal zone, with these

regions typically sharing a common species pool

(Kuklinski & Barnes, 2008). However, none of these

descriptions particularly relate to the Baltic Sea, a

typically brackish environment in which benthic

communities are composed of opportunistic species.

Therefore, we anticipate that the stressful conditions

of the brackish hydrolittoral zone will lead to a lower

species diversity of predominately opportunistic

organisms and assemblages, as found in the adjacent

littoral zone. The higher salinity in the transient

environment between the Baltic Sea and North Sea

together with Atlantic Ocean-induced waves, tides and

sea level changes may lead to an increased difference

between hydrolittoral and littoral assemblages, as a

result of the appearance of marine species. In this

circumstance, intertidal–hydrolittoral specialists from

temperate fully marine systems (such as the North

Sea) might be expected to contribute to independent

hydrolittoral assemblages. The higher frequency of

occurrence of encrusting species in the hydrolittoral in

higher salinity could be due to random movement of

the species originally inhabiting the adjacent littoral

environment. This increased probability is likely to be

independent of the rock size, which is otherwise a

limiting factor for encrusting community development

298 Hydrobiologia (2016) 765:297–315

123

(Grzelak & Kuklinski, 2010). In this study, the

sampling in the hydrolittoral zone was performed

concomitantly with sampling in the adjacent littoral

zones, allowing a robust comparative analysis

between the features of faunal assemblages in both

zones along the Baltic Sea coast. To our knowledge,

this study is the first investigation of encrusting fauna

within the hydrolittoral zone on such a scale in the

Baltic Sea.

Materials and methods

Study sites and sampling

To assess the large-scale patterns of the hard-bottom

encrusting assemblages structure, we selected 14

locations along the Swedish and Norwegian Baltic

Sea rocky shore between Tore (Sweden) (65�530N,22�420E) and Lillesand (Norway) (58�150N, 08�290E)(Fig. 1). Locations were labelled chronologically

based on their geographical position and sampling

order starting from the Bothnian Bay (B01–B05)

surveyed in August 2007 through the west coast of

Baltic Proper (B06–B09) to the Kattegat and Skager-

rak (B10–B14) sampled in October 2007. During the

survey, environmental variables such as salinity and

temperature were measured. Water salinity ranged

from 0.5 in the Bothnian Bay to over 27 in Kattegat

and Skagerrak, and the temperature ranged between 13

and 15�C in Bothnian Bay (August) and between 8 and

10�C in the Baltic Proper and Kattegat and Skagerrak

(October). These measurements follow the multi-year

(10 years) surface temperatures and salinity data

[derived for the purpose of this study from the World

Ocean Database Select and Search and computed with

the use of the Ocean Data View software (Schlitzer,

2015, Germany) (see Fig. 1)].

To compare the structure of encrusting assemblages

in the shallow Baltic Sea rocky habitat, rock samples

from two marine coastal zones (hydrolittoral and

littoral) were collected concomitantly. The Baltic Sea

is regarded as non-tidal; however, there are daily mean

sea level variations estimated to be between 17 and

18 cm at the Baltic Proper (Suursaar & Kullas, 2006).

Stations B11 to B14, located in the area of Skagerrak

and Kattegat, are micro-tidal areas with astronomical

tidal ranges of 20–30 cm and approximately 40 cm,

respectively (Cossellu & Nordberg, 2010). The sea

level range in the non-tidal area almost overlaps with

the tidal range in the micro-tidal area. Therefore, for

the purpose of this study, we used a uniform termi-

nology to describe the two sampling zones across tidal

and no tidal areas (hydrolittoral and littoral).

Hydrolittoral samples were collected by hand from

the seashore at mean sea level in non-tidal areas and at

Fig. 1 Map of the study

area system with marked

sampling locations and

salinity in situ values

measured at the time of

sample collection plotted on

multi-year surface salinity

data. Multi-year surface

salinity data were derived

from the World Ocean

Database Select and Search

and computed with use of

the Ocean Data View

software

Hydrobiologia (2016) 765:297–315 299

123

appropriately the extreme low water spring (ELWS)

tide level in tidal areas. The mean sea level at non-tidal

locations was evaluated by the position of the vege-

tation line marked by marine and land flora (Kautsky

et al., 1986). Rock samples were collected at the same

time by SCUBA in the shallow littoral zone from

a * 3-m depth. At each level of the coastal habitat

(hydrolittoral and littoral), three subsamples (sepa-

rated by approximately 5 m) consisting of rocks of

various sizes were collected randomly at each location

to obtain examples of the possible rock size variants.

The average number of rocks collected per subsample

at each location in the hydrolittoral zone varied from

17 to 22, whereas in the littoral zone the number of

rocks varied from 33 to 96. The average rock size per

subsample varied between locations and ranged from

94 to 332 cm2 and from 65 to 220 cm2 in hydrolittoral

and littoral zones, respectively. The surface area of

each rock was measured with an inelastic net gridded

with 2 cm2, and the percentage cover of fauna and

flora on each rock was estimated based on the ratio

between covered and bare rock surface. Organisms

were identified to the lowest possible taxonomic level,

typically to the species level and counted (individuals

per m2). The sampling effort was tested using cumu-

lative plots where the number of observed encrusting

species was plotted versus the number of rocks

(PRIMER 6TM routine) for the locations within the

hydrolittoral and littoral zones. The results from each

of the locations were combined for a collective figure

(SigmaPlot10.0 software) representing the whole

study area.

Data analysis

Faunal data from each subsample were analysed for

species richness, abundance (individuals per m2), the

Shannon–Wiener (H0) proportional diversity index

(log base 10) and Pielou’s evenness index (compare

the species abundances in communities). The diversity

indices take into account information on both species

richness and abundance obtained from measuring the

heterogeneity of encrusting assemblages. These

results were presented graphically as averaged values

(± SE).

The relationship between encrusting assemblages,

represented by the total abundance (ind/m2) and

environmental variables, was studied using a canon-

ical correspondence analysis (CCA) with CANOCO

software. The analysis was performed on raw abun-

dance data and the untransformed matrix of environ-

mental variables. A selection of variables (salinity,

habitat type, wave exposure, mean rock size, temper-

ature, latitude and longitude) was used to best explain

the variance of the biological data based on the

encrusting species number and abundance. Latitude

and longitude were used as covariables. The signifi-

cance of each variable was estimated in a Monte Carlo

test using 999 permutations. For the purpose of the

CCA, wave exposure data were obtained for each

sampling location. The wave exposure grid covering

the Baltic Sea area was constructed from a combined

Simplified Wave Model method and the off-shore

significant wave height was modelled with MIKE2

using the calculations included in the 2010 AquaBiota

report (Wijkmark & Isæus, 2010). According to this

source, which reports eight classes of wave exposure

levels (from ultra-sheltered to extremely exposed), the

wave exposure at our surveyed locations varied over

the spatial scale and was rated from sheltered through

moderately exposed to exposed, in the Bothnian Bay

(locations B01, B02, B04 and B06), central Baltic Sea

(locations B03, B05, B07–B10) and Kattegat and

Skagerrak (locations B11–B14), respectively. These

west-to-east gradients were also accompanied by

decreasing tidal amplitude.

The analysis of covariance (ANCOVA) was used to

test the effect of salinity and habitat (two levels) on the

diversity parameters (species richness, Shannon–

Wiener diversity, Pielou’s evenness, percent cover of

fauna and abundance). Prior to running parametric

tests, we tested for homogeneity of variance among

samples with Levene’s test. For the ANCOVA anal-

ysis, we used habitat level as a grouping variable and

salinity as a covariate.

To investigate the effect of the increasing salinity

gradient within the Baltic system, faunal assemblages

from all subsamples collected at the study locations were

compared using a resemblance matrix on square-root

transformed data based on Bray–Curtis similarity. Non-

metric multidimensional scaling (nMDS) was conducted

using the PRIMER 6TM package (Plymouth Routines In

Multivariate Ecological Research, PRIMER-E Ltd).

Differences in community structure between hydrolit-

toral and littoral were mapped with nMDSs and tested

with analysis of similarity (ANOSIM).

To illustrate the relationship between substratum

sizes and encrusting assemblages from the

300 Hydrobiologia (2016) 765:297–315

123

hydrolittoral and littoral zones, we segregated the

samples according to the rock size into eight groups

and compared frequencies of occurrence of encrusting

organisms within the different-sized rock groups. To

illustrate the probability of species occurrence in

relation to rock size range, the frequency of occur-

rence based on a presence/absence ratio (± standard

error) was estimated for a given rock size range (100,

200, 300, 400, 500, 600, 700 and 800 cm2) for the

hydrolittoral zone and compared with the results from

the littoral zone. The frequency (mean value ± SE) of

species occurrence was plotted against the rock size

classes for each location. The assemblage structure

differences between habitats based on the species

abundance data within the rock size groups as samples

were illustrated with nMDS ordination plots and tested

with analysis of similarity (ANOSIM).

Results

A total of 24 encrusting taxa were found at 14

sampling locations. At location B01, no encrusting

assemblages were recorded in the hydrolittoral and

littoral zones and at B02 none were found in the littoral

zone; these locations were thus not considered further

in this study. For samples collected in the hydrolittoral

zone, we identified 21 species (nine bryozoans, six

annelids, three barnacles and four other), and for the

shallow littoral zone, we identified 24 species (11

bryozoans, six annelids, three barnacles and four

other). The complete list of the species and their

abundances is presented in Table 1. Accumulation

curves for species from locations B02–B10 in the

hydrolittoral zone and B03–B09 in the littoral zone

(Fig. 2) were asymptotic. For other locations, species

accumulation curves showed a continued slight

increase.

Spatial patterns of species richness in the hydrolit-

toral zone resembled those found in the littoral

assemblages. At the locations situated between the

Bothnia Bay and the Baltic Proper (with the exception

of locations B05 and B06), species richness was lower

than at locations from B10 to B14 (Fig. 3). The mean

abundance of encrusting organisms in hydrolittoral

and littoral zones varied through space and varied

from only a few individuals per m2 (location B02) up

to over 30,000 (locations B10 and B14). The mean

abundance in general was higher at locations with a

higher salinity, both in the hydrolittoral and littoral

zones. In the brackish Bothnian Bay, Baltic Proper and

Kattegat (locations from B03 to B10), the abundance

of assemblages from the littoral zone exceeded

hydrolittoral assemblages; however, the trend was

reversed in the locations with the highest salinity

(B11–B14). The results of Pielou’s measure of even-

ness shows that, in general, communities occurring in

low salinity (B03–B09) were characterized by higher

variation compared to marine communities (B10–

B14). However, the values of the evenness index

between habitats showed a stronger diversification at

locations with low salinity levels and low species

number (locations B02–B10), than at locations with

higher salinity and species number (locations B11–

B14), and the index presented similar values (Fig. 3).

Results of analysis of covariance (ANCOVA) showed

that the structure of encrusting assemblages varied

significantly as a result of salinity change in terms of

species richness, abundance, faunal cover and diver-

sity (Table 2). Assemblages differed between habitats

(hydrolittoral versus littoral) significantly only in

terms of species richness (F = 23.78, P\ 0.001).

The canonical correspondence analysis (CCA)

showed strong relationship between encrusting assem-

blages and environmental parameters (Fig. 4). The

Monte Carlo permutation test for the first axis was

significant (F = 7.494, P = 0.017). According to the

results of the analysis, salinity was the most significant

factor affecting assemblage structure (F = 10.182,

P = 0.001). However, there were other factors that

had lower but also considerable impacts on overall

species composition and community structure. For

example, flora coverage (F = 5.846, P = 0.001),

wave exposure (F = 6.120, P = 0.001), mean rock

size (F = 2.655, P = 0.025) and habitat type

(F = 8.847, P = 0.001) (which was a nominal value)

were also statistically significant. Overall, 98.7% of

the correlation between species and continuous vari-

ables was explained by the first axis of the CCA

diagram (F = 8.762, P = 0.001; Eigenval-

ues = 2.719; Total inertia = 3.414). Remaining

tested variables (temperature and fauna coverage)

were not statistically significant and did not appear to

have an influence on community structure.

The overall number of species in the hydrolittoral

zone was lower than in the littoral and a great majority

of the species were found in both habitats (Table 1).

Hydrolittoral assemblages in the brackish part of the

Hydrobiologia (2016) 765:297–315 301

123

Table

1Encrustingspeciesrecorded

inhydrolittoralandlittoraloftheBalticSea

Location

B01

B02

B03

Phylum

Taxa

Hydrolittoral

Hydrolittoral

Littoral

Hydrolittoral

Littoral

Cnidaria

Hydrozoa(Linnaeus,1758)

Foraminifera

Annelida

Circeis

spirillum

(Linnaeus,1758)

Januapagenstecheri(Q

uatrefages,1865)

Laeospiracorallinae(deSilva&

Knight-Jones,1962)

Spirobranchustriqueter

(Linnaeus,1758)

Spirorbis

spirorbis

(Linnaeus,1758)

Spirorbis

tridentatus(Levinsen,1883)

Arthropoda

Amphibalanusimprovisus(D

arwin,1854)

20.11±

3.56

4.56±

6.40

Sem

ibalanusbalanoides

(Linnaeus,1767)

Verruca

stroem

ia

(O.F.Muller,1776)

Bryozoa

Aetea

truncata

(Lam

ouroux,1812)

Callopora

lineata

(Linnaeus,1767)

Celleporellahyalina(Linnaeus,1767)

Cribrilinaannulata

(O.Fabricius,1780)

Cribrilinacryptooecium

(Norm

an,1903)

Cribrilinapunctata

(Hassall,1841)

Cryptosula

pallasiana(M

oll,1803)

Einhornia

crustulenta

(Pallas,1766)

2.09±

3.63

113.94±

165.86

Electra

pilosa

(Linnaeus,1767)

Escharellaimmersa

(Fleming,1828)

Scrupocellariareptans(Linnaeus,1758)

Mollusca

Modiolusmodiolus(Linnaeus,1758)

Mytilus(Linnaeus,1758)

302 Hydrobiologia (2016) 765:297–315

123

Table

1continued

Location

B04

B05

B06

Phylum

Taxa

Hydrolittoral

Littoral

Hydrolittoral

Littoral

Hydrolittoral

Littoral

Cnidaria

Hydrozoa(Linnaeus,1758)

Foraminifera

Annelida

Circeis

spirillum

(Linnaeus,1758)

Januapagenstecheri(Q

uatrefages,1865)

Laeospiracorallinae(deSilva&

Knight-Jones,1962)

Spirobranchustriqueter

(Linnaeus,1758)

Spirorbis

spirorbis

(Linnaeus,1758)

Spirorbis

tridentatus(Levinsen,1883)

Arthropoda

Amphibalanusimprovisus(D

arwin,1854)

13.50±

2.09

25.90±

7.50

18.36±

5.08

142.35±

171.20

9.64±

3.13

48.34±

28.17

Sem

ibalanusbalanoides

(Linnaeus,1767)

Verruca

stroem

ia

(O.F.Muller,1776)

Bryozoa

Aetea

truncata

(Lam

ouroux,1812)

Callopora

lineata

(Linnaeus,1767)

Celleporellahyalina(Linnaeus,1767)

Cribrilinaannulata

(O.Fabricius,1780)

Cribrilinacryptooecium

(Norm

an,1903)

Cribrilinapunctata

(Hassall,1841)

Cryptosula

pallasiana(M

oll,1803)

Einhornia

crustulenta

(Pallas,1766)

2555.25±

1092.34

40.02±

29.51

761.74±

499.10

1703.94±

195.16

Electra

pilosa

(Linnaeus,1767)

10.16±

17.59

4.81±

8.32

1.09±

1.89

Escharellaimmersa

(Fleming,1828)

Scrupocellariareptans(Linnaeus,1758)

Mollusca

Modiolusmodiolus(Linnaeus,1758)

Mytilus(Linnaeus,1758)

0.58±

1.01

5.86±

4.05

309.69±

95.23

Hydrobiologia (2016) 765:297–315 303

123

Table

1continued

Location

B07

B08

B09

B10

Phylum

Taxa

Hydrolittoral

Littoral

Hydrolittoral

Littoral

Hydrolittoral

Littoral

Hydrolittoral

Littoral

Cnidaria

Hydrozoa(Linnaeus,1758)

1.30±

1.36

Foraminifera

Annelida

Circeis

spirillum

(Linnaeus,1758)

Januapagenstecheri(Q

uatrefages,

1865)

Laeospiracorallinae(deSilva&

Knight-Jones,1962)

0.60±

1.03

Spirobranchustriqueter

(Linnaeus,

1758)

Spirorbisspirorbis

(Linnaeus,1758)

2.79±

3.84

Spirorbis

tridentatus(Levinsen,1883)

Arthropoda

Amphibalanusimprovisus(D

arwin,

1854)

48.14±35.57

1.78±3.078

0.62±1.08

167.28±217.85

819.89

±375.73

26227.41

±7533.42

Sem

ibalanusbalanoides

(Linnaeus,1767)

Verruca

stroem

ia

(O.F.Muller,1776)

Bryozoa

Aetea

truncata

(Lam

ouroux,1812)

0.45±

0.78

Callopora

lineata

(Linnaeus,1767)

14.21±

13.07

Celleporellahyalina(Linnaeus,1767)

Cribrilinaannulata

(O.Fabricius,1780)

Cribrilinacryptooecium

(Norm

an,

1903)

0.90±

1.56

Cribrilinapunctata

(Hassall,1841)

Cryptosula

pallasiana(M

oll,1803)

Einhornia

crustulenta

(Pallas,1766)

679.24±

244.52

367.75±

293.60

191.12±

179.94

16.18±

14.26

Electra

pilosa

(Linnaeus,1767)

69.12±

79.67

32.11±

27.74

Escharellaimmersa

(Fleming,1828)

Scrupocellariareptans(Linnaeus,

1758)

Mollusca

Modiolusmodiolus(Linnaeus,1758)

Mytilus(Linnaeus,1758)

4.74±

4.35

484.96±

190.4

41.82±

40.87

426.53±

90.46

206.09±

106.38

55.38±

65.79

202.85±

31.90

2652.46±

1446.9

304 Hydrobiologia (2016) 765:297–315

123

Table

1continued

Location

B11

B12

B13

B14

Phylum

Taxa

Hydrolittoral

Littoral

Hydrolittoral

Littoral

Hydrolittoral

Littoral

Hydrolittoral

Littoral

Cnidaria

Hydrozoa

(Linnaeus,1758)

49.58±

85.86

41.17±

63.93

87.34±

89.51

21.63±

0.21

3.66±

6.34

3.88±

0.34

179.40±

310.73

0.74±

1.29

Foraminifera

125.86±

217.99

5.71±

2.36

1.42±

2.46

200.92±

148.97

57.62±

97.62

295.38±

60.78

63.87±

49.66

248.57±

189.23

Annelida

Circeis

spirillum

(Linnaeus,1758)

1.31±

2.27

128.07±

219.62

Janua

pagenstecheri

(Quatrefages,

1865)

702.54±

1188.99

216.42±

374.85

873.97±

1384.30

60.16±

31.79

9643.99±

15863.01

17709.07±

13794.14

427.52±

735.22

Laeospira

corallinae(de

Silva&

Knight-

Jones,1962)

35.38±

61.27

12.39±

20.06

128.23±

209.84

27.08±

8.46

7133.42±

11067.06

0.35±

0.60

3308.64±

1645.84

197.39±

318.04

Spirobranchus

triqueter

(Linnaeus,1758)

1.16±

2.01

38.28±

30.58

2.37±

4.11

0.35±

0.61

5.04±

3.40

Spirorbisspirorbis

(Linnaeus,1758)

116.08±

168.16

513.53±

392.82

275.36±

400.97

541.36±

236.15

84.16±

54.35

907.99±

898.71

2134.99±

1930.31

5271.35±

5921.17

Spirorbis

tridentatus

(Levinsen,1883)

62.45±

94.87

3843.36±

4336.96

3263.41±

2110.46

793.38±

325.29

41.04±

40.95

1486.87±

1024.16

4630.51±

4429.5

11372.41±

8370.76

Arthropoda

Amphibalanus

improvisus

(Darwin,1854)

3444.96±

2100.81

80.96±

70.74

977.18±

640.92

3.18±

1.18

105.80±

123.39

2.13±

2.74

28.22±

33.61

0.43±

0.74

Sem

ibalanus

balanoides

(Linnaeus,1767)

28.78±

49.84

1.37±

2.37

14.65±

9.3

4.85±

8.40

21.37±

37.01

73.30±

126.96

1.12±

1.93

Verruca

stroem

ia

(O.F.Muller,1776)

1.91±

3.30

0.46±

0.79

26.24±

11.04

22.27±

9.09

1.19±

2.06

1.65±

1.44

119.53±

61.37

870.01±

1440.36

Bryozoa

Aetea

truncata

(Lam

ouroux,

1812)

4.26±

4.35

131.70±

124.11

0.37±

0.64

Callopora

lineata

(Linnaeus,1767)

12.87±

11.71

89.94±

48.84

53.36±

84.64

6.41±

11.10

38.74±

34.06

234.27±

275.56

4.26±

7.38

Celleporella

hyalina

(Linnaeus,1767)

2.14±

2.75

38.88±

64.09

1.65±

1.97

Cribrilinaannulata

(O.Fabricius,

1780)

3.81±

6.61

6.92±

6.01

26.59±

7.34

3205.07±

3442.44

3.93±

4.13

9.18±

5.69

12.97±

16.69

79.40±

63.32

Hydrobiologia (2016) 765:297–315 305

123

Baltic Sea including Bothnian Bay and Baltic Proper

locations (locations B02–B09) were composed of four

opportunistic species: Amphibalanus improvisus (Dar-

win, 1854), Einhornia crustulenta (Pallas, 1766),

Electra pilosa (Linnaeus, 1767) and Mytilus juv.

(Linnaeus, 1758), which were distributed heteroge-

neously between the locations. Those species, as

indicated by the CCA (Fig. 4), show tolerance to low

salinity. The hydrolittoral assemblages at the Bothnian

Bay and the northern part of Baltic Proper (B02–B06)

were dominated mainly by A. improvisus.Mytilus juv.

contributed significantly to assemblage abundance in

the Baltic Proper (locations B07–B09) and was an

important component of marine encrusting assem-

blages (locations B10–B14). E. crustulenta dominated

littoral assemblages and was a rare component of

hydrolittoral assemblages (locations B02, B05 and

B11 only). Among the species observed in this Baltic

Sea region (B04–B06), there was one—Electra

pilosa—that occurred in the hydrolittoral zone and

did not appear in the nearby shallow littoral assem-

blages. E. pilosa also appeared in the marine littoral

zone (B11–B14); however, the average numbers in

both zones were very low (\ 50 individuals per m2). In

the Baltic Sea–North Sea transition (locations B10),

both hydrolittoral and littoral assemblages were dom-

inated by A. improvisus. This species (A. improvisus)

was also observed in much lower numbers at locations

B11–B14 (Kattegat and Skagerrak) and its abundance

was much higher in hydrolittoral compared to littoral.

At this part of the studied area (locations B11–B14),

assemblages had greater species diversity due to (1)

specialized species which were found in the hydrolit-

toral zone (e.g. Janua pagenstecheri (Quatrefages,

1865), Laeospira corallinae (de Silva and Knight

Jones, 1962), Semibalanus balanoides (Linnaeus,

1767) or Cryptosula pallasiana (Moll, 1803)) and

(2) the high number of species occurring abundantly in

the littoral zone (e.g. Spirorbis spirorbis (Linnaeus,

1758), Einhornia crustulenta or Escharella immersa

(Fleming, 1828)). Additionally, there were a few

species that occurred only in the littoral zone (the

bryozoans Aetea truncata (Lamouroux, 1812) and

Scrupocellaria reptans (Linnaeus, 1758) and the

mollusc Modiolus modiolus (Linnaeus, 1758)). A

few species were also found to be specific to the

hydrolittoral zone and were present only in very low

numbers (Table 1). Hydrolittoral and littoral encrust-

ing assemblages also differed in terms of theTable

1continued

Location

B11

B12

B13

B14

Phylum

Taxa

Hydrolittoral

Littoral

Hydrolittoral

Littoral

Hydrolittoral

Littoral

Hydrolittoral

Littoral

Cribrilinacryptooecium

(Norm

an,

1903)

89.37±

82.03

58.30±

26.25

2.75±

4.76

195.54±

83.13

211.96±

307.18

200.61±

212.00

Cribrilinapunctata

(Hassall,1841)

3.81±

6.66

37.65±

30.08

24.92±

28.09

42.41±

22.66

29.01±

12.68

7.72±

13.36

8.52±

10.97

Cryptosula

pallasiana(M

oll,1803)

30.27±

26.91

22.34±

8.90

1020.38±

145.23

185.11±

83.41

37.55±

65.03

98.50±

82.38

2469.80±

1596.23

200.60±

208.99

Einhornia

crustulenta

(Pallas,1766)

1.91±

3.30

3.48±

6.02

Electra

pilosa

(Linnaeus,1767)

7.63±

13.21

23.86±

19.34

46.76±

66.69

12.93±

8.16

9.39±

8.11

3.19±

2.94

10.54±

10.24

Escharellaimmersa

(Fleming,1828)

2.28±

2.67

80.50±

69.9

9.50±

8.26

6.31±

10.93

825.82±

1358.41

Scrupocellariareptans(Linnaeus,1758)

4.86±

1.12

56.79±

92.63

Mollusca

Modiolusmodiolus(Linnaeus,1758)

319.84±

196.32

55.37±

54.27

Mytilus(Linnaeus,1758)

136.68±

20.67

105.36±

50.06

51.35±

38.17

62.35±

29.35

21.77±

31.34

321.80±

392.37

54.10±

80.94

28.51±

24.76

Values

expressed

asmeanabundance

(indiv./m

2±

SD),locationlabelswithaccordance

toFig.1

306 Hydrobiologia (2016) 765:297–315

123

contribution of taxonomic groups to the relative

abundance. Samples from the brackish parts of the

Baltic Sea (the Bothnian Bay and Baltic Proper) were

dominated by arthropods and molluscs. For the

corresponding littoral assemblages, there was a greater

proportion of bryozoans. In higher salinity (locations

B10–B14), serpulid worms contributed significantly to

both hydrolittoral and littoral assemblages.

An overall nMDS ordination presenting distribu-

tion of all assemblages showed differences in the

structure of assemblages between hydrolittoral and

littoral zones (Fig. 5). Analysis of similarity (ANO-

SIM) performed to test the differences in assemblages

between habitats showed low but significant separa-

tion between hydrolittoral and littoral (Global

R = 0.151, P\ 0.001). In detailed comparison, the

frequency of fauna occurrence in the littoral samples

was higher in most of the rock size classes compared to

those in the hydrolittoral samples (Fig. 6). The

frequency of occurrence of encrusting organisms

equalled 1, regardless of habitat and rock size, in

higher salinity (B10–B14). Occurrence of encrusting

fauna in relation to rock size differed between

hydrolittoral and littoral zones (Fig. 6). In lower

salinity, where diversity was low, the negative effect

of ‘‘small rocks’’ on frequency of encrusting species

occurrence was stronger in the hydrolittoral compared

to littoral zone. In general, the probability of finding

encrusting fauna increased with the rock size and was

higher in littoral zones, where at most of the salinity

levels even small rocks had a higher probability of

encrustation. Based on the results of the nMDS and

ANOSIM performed for each location, the assem-

blages occurring in hydrolittoral zones were generally

different from those of the littoral zones, although the

effect of rock size was less significant at locations in

the brackish Baltic Sea (location B03–B09) (Fig. 7).

Assemblages from the North Sea–Baltic Sea (loca-

tions B11–B14) transition zone distinguished between

the hydrolittoral and littoral habitats for each of the

rock size class. Results of ANOSIM tests for assem-

blages at given rock size range performed for each

location generally showed moderate and high separa-

tion between hydrolittoral and littoral assemblages.

Discussion

In this study, we investigated encrusting assemblages

inhabiting rocks in the Baltic Sea hydrolittoral zone in

comparison to the adjacent littoral zone along a

salinity gradient. Comparative measurement of bio-

logical parameters describing encrusting assemblages

inhabiting the Baltic Sea hydrolittoral and littoral

zones (such as species richness, abundance, diversity,

percentage cover of fauna) indicated the significant

role of local dispersal limitations in encrusting species

composition and a strong influence of nearby biotopes.

Table 2 The results of the analysis of covariance (ANCOVA) testing the effects of salinity and habitat on the basic community

parameters (significant 636 differences are highlighted in bold) where habitat was used as a grouping factor while salinity as covariate

Degr. of freedom Species richness Shannon diversity Pielou evenness

SS MS F P SS MS F P SS MS F P

Intercept 1 1.08 1.08 13.77 <0.001 0.02 0.02 0.77 0.38 2.54 2.54 25.05 <0.001

Salinity 1 27.55 27.55 351.41 <0.001 2.82 2.82 125.96 <0.001 0.52 0.52 5.17 0.03

Habitat 1 1.86 1.86 23.78 <0.001 0.07 0.07 3.19 0.08 0.08 0.08 0.77 0.38

Error 75 5.88 0.08 1.68 0.02 7.61 0.10

Total 77 35.30 4.58 8.22

Degr. of freedom Coverage Abundance

SS MS F P SS MS F P

Intercept 1 25.17 25.17 0.25 0.62 85033346.87 85033346.87 1.05 0.31

Salinity 1 2391.44 2391.44 24.00 <0.001 2301379851.97 2301379851.97 28.49 <0.001

Habitat 1 212.60 212.60 2.13 0.15 11480841.35 11480841.35 0.14 0.71

Error 75 7473.86 99.65 6057874913.05 80771665.51

Total 77 10077.90 8370735606.37

Hydrobiologia (2016) 765:297–315 307

123

Over the scale of the entire Baltic Sea, spatial species

distribution is controlled mainly by the steep salinity

gradient (Herkul et al., 2006; Zettler et al., 2014),

which, according to the results of this study, is also

observed in our data and matched our predictions.

Along the gradient of increasing salinity, the spatial

trends in the hydrolittoral zone, including species

composition and increased diversity of encrusting

assemblages, were found to be similar to those

reported for other macrobenthic communities from

deeper regions of the Baltic Sea (Bonsdorff & Pearson,

1999;Westerbom et al., 2002) and in particular, as this

study clearly indicated, the nearby littoral. Similar

correlation between the salinity and the species

richness and abundance of encrusting assemblages

was noted for other taxonomic and functional groups

(e.g. Darr et al., 2014; Zettler et al., 2014).

Among the environmental variables we studied

(including temperature, mean rock size, wave expo-

sure or percent coverage by fauna), salinity showed the

strongest relationship with the large-scale pattern of

encrusting assemblages. Low salinity in areas addi-

tionally exposed to harsh winter conditions and ice

formation appeared to inhibit the development of

hydrolittoral communities but favoured species

adapted to harsh conditions. The structure of the

encrusting assemblages in the brackish environment of

the Baltic Sea consisted of four main species: A.

improvisus, Mytilus juv., Einhornia crustulenta and

Electra pilosa. Such homogeneity of species

composition was recorded over a large scale along

the salinity gradient and was also evident in the values

of the Shannon–Wiener and Pielou’s indices (Fig. 3).

This complementary information indicates that the

brackish encrusting assemblages (stations B02 to B09)

were generally represented by fewer (although highly

abundant) species, in contrast to assemblages recorded

from more saline environments (B11 to B14), where

communities are more species rich with a few

dominant species (with the rest of species considered

to be rare in terms of abundance (Fig. 3, Table 1)).

Although the structure of the hydrolittoral and littoral

assemblages in the brackish environment of the

Bothnian Bay and the Baltic Proper remained homo-

geneous over this large area, hydrolittoral assemblages

(in contrast to littoral) were enriched by the episodic

appearance of the bryozoan Electra pilosa. The most

frequent components of the brackish hydrolittoral

assemblages, represented by barnacles andmussels (A.

improvisus and Mytilus juv.), have been observed in

high biomass on exposed shores of the Baltic Sea

(Wallin et al., 2011) and were considered to be the

most frequent components of wave-exposed intertidal

biotopes in the Northern Atlantic Ocean bioregion

(Bartsch & Tittley, 2004). This confirms that A.

improvisus is well adapted for survival in the highly

hydrodynamic coastal rock belt of the Baltic Sea and is

one of the dominant species in brackish communities.

Similar observations have been made for another

barnacle species from the Canadian coast, suggesting

Fig. 2 Species accumulation plots in hydrolittoral (left) and littoral (right) for the study locations. Location labels are in accordance

with Fig. 1

308 Hydrobiologia (2016) 765:297–315

123

Fig. 3 Comparison of basic

diversity parameters:

a species richness,

b abundance, c percentcoverage by fauna, d)Shannon–Wenner diversity

and e evenness indexpresented as mean

values ± standard error

between hydrolittoral and

littoral assemblages.

Location and salinity labels

are in accordance with

Fig. 1

Hydrobiologia (2016) 765:297–315 309

123

that barnacles are better adapted to survive harsh

winter ice scour than other species (Heaven &

Scrosati, 2008). The lack of adult individuals of

Mytilus species indicates that some factors (e.g. wave

action, salinity and predation) of this zone may

prevent this species from reaching maturity. Where

the salinity is higher, opportunistic species, especially

Mytilus juv. are replaced by stenohaline marine

species, particularly bryozoans and serpulids

(Table 1). As a result of appearance of marine species,

including common intertidal taxa (e.g. L. corallinae, S.

balanoides), we observed increased species diversity

in the Baltic Sea–North Sea transition zone (the

Sound—location B10) and marine locations, Kattegat

and Skagerrak (locations B11–B14), both in the

hydrolittoral and littoral encrusting assemblages. In

general, there was a lower species richness and

abundance in the hydrolittoral assemblages compared

with the adjacent littoral zone (Fig. 3), and although

there were a few exceptions, these assemblages shared

a common species pool, with none of the abundant

species were specific to the hydrolittoral zone. Despite

sharing species composition similarities, these com-

munities differed in their dominant species; the higher

occurrence of A. improvisus and Mytilus juv. were

attributed to hydrolittoral assemblages (except for the

marine locations B12–B14), while littoral assem-

blages were dominated by bryozoans and polychaetes

(Table 1). Although the hydrolittoral zone of the

Baltic Sea has distinct encrusting faunal assemblages,

especially towards more saline water locations, they

do not seem to be fully independent and it is possible

that they have originated from the adjacent littoral

zone.

The species richness and diversity variability across

the land–sea gradient has been the subject of a number

of studies in tidal basins where the effects of water

level elevation on sessile species diversity were

compared (e.g. Scrosati et al., 2011). These studies

concluded that the structure of sessile assemblages

varied in relation to elevation and exposure. In this

study, the lower abundance observed in the Baltic Sea

hydrolittoral assemblages, and the lower species

richness compared to nearby littoral assemblages,

appears to be caused by disturbances related to coastal

dynamics and the less favourable conditions for

community development (Herkul et al., 2006; Balata

& Luigi, 2008; Kuklinski & Barnes, 2008; Kuklinski,

2009;Wiklund et al., 2012). Although the Baltic Sea is

not tidal, Wiklund et al. (2012) suggested that wave

impacts on spring hydrolittoral communities in the

Baltic Sea are comparable to those observed in the

oceanic areas. Seasonal variability in wave activity,

enhanced by increased hydrodynamic forcing during

the winter and early spring in the coastal area

(Wiklund et al., 2012), leads to a reduction in marine

populations by impeding the full development of

benthic communities and may be a reason for the

distinctive nature of the hydrolittoral communities. A

northward gradient of decreasing salinity and changes

in climate conditions (e.g. decreasing temperature)

may explain the rapid decline in abundance and

percentage cover of fauna in the hydrolittoral com-

pared with analogous littoral assemblages elsewhere.

Long and extensive ice presence, which, for the

northern Baltic Sea, can exceed 150 days annually,

Fig. 4 Canonical correspondence analysis (CCA) plot for all

encrusting species from selected environmental variables:

salinity, wave exposure (wave exp), mean rock size (mean

roc), flora coverage (flora co) (arrows) and habitat (depth zo)

(triangular) represented by nominal value. The percentage of

variability explained by the axes is given. Abbreviations regard

following taxa: At Aetea truncata, Can Cribrilina annulata, Pt

Spirobranchus triqueter, Cpun Cribrilina punctata, Eimm

Escharella immersa, Srep Scrupocellaria reptans, Cs Circeis

spirillum, Ss Spirorbis spirorbis, Vs Verruca stroemia, Ccry

Cribrilina cryptooecium, Mm Modiolus modiolus, St Spirorbis

tridentatus, Clin Callopora lineata, Epil Electra pilosa, M

Mytilus, Bi Amphibalanus improvisus, Ecrus Einhornia crustu-

lenta, Cpal Cryptosula pallasiana, Sb Semibalanus balanoides,

Chya Celleporella hyalina, Jp Janua pagenstecheri, Lc

Laeospira corallinae, Ds Hydrozoa

310 Hydrobiologia (2016) 765:297–315

123

causes severe ice scouring on rocky habitats, espe-

cially in the shallowest areas (Scrosati & Heaven,

2007). For hydrolittoral rock encrusting assemblages,

this result in seasonal scouring, preventing the forma-

tion of multi-year communities and resulting in

assemblages composed of young, small organisms.

The lack of adult individuals of bivalve Mytilus sp. in

the hydrolittoral is likely to be caused by such frequent

disturbance (Sousa, 1979), explaining low abundance

and low percentage coverage by fauna. Additionally,

the irregular nature of water level changes also

contributes to the scarcity of fauna.

Local heterogeneity can be a result of many factors

such as biological adaptations of particular encrusting

species (such as the small, hard shell barnacle A.

improvisus or bryozoan E. crustulenta), discontinuous

availability of substrate or dynamic coastal conditions.

The significant differences between assemblages from

hydrolittoral and littoral sites of similar salinity could

be due to the contribution of the general sediment

characteristics at sampling sites and the way rocks are

oriented on the sediment. The properties of the

substrate and surrounding sediment can influence flora

and fauna occurrence at the hard bottom (Bucas et al.,

2007). Comparison of relative frequencies of occur-

rence of encrusting species in hydrolittoral and littoral

samples in relation to the rock size indicated that this

was lowest for small rocks in the shallow hydrolittoral.

At the same time, it was noticeable that similar-sized

rocks in the littoral zone were more frequently

overgrown. Multivariate analysis presenting faunal

groups according to rock size also illustrated differ-

entiation between assemblages from the two coastal

marine habitats and a distinction between hydrolittoral

and littoral zones in the western part of the Baltic Sea

(Fig. 7). As indicated in a previous study, rock size

and its susceptibility to agitation affect epibenthic

community development by regulating their abun-

dance and taxonomic diversity (Kuklinski et al.,

2005). Small rocks are known to be more sensitive

to overturning and scouring as a result of physical

disturbance than larger substrates (Gedan et al., 2011),

and therefore, a low frequency of species occurrence

on this substrate is understandable (this tendency was

recorded in our observations). Similar to the previous

studies, we observed that a lower percentage of faunal

coverage of rock surfaces was recorded within smaller

boulders as a result of limitations of space for

colonization and higher rate of mortality caused by

disturbances, especially when they were surrounded

by mobile sediment (Sousa, 1979; Bucas et al., 2007).

Similarly to our results (Fig. 6), Grzelak & Kuklinski

(2010) found a higher probability of the presence of

organisms on large and medium rocks than on small

rocks, confirming that in the Baltic Sea coastal habitat

larger rocks are more stable and likely to provide a

better substrate for community development (Liver-

sage & Kotta, 2015). In higher salinity, where

Fig. 5 Comparison (non-

metric multidimensional

scaling) of the encrusting

assemblages in different

salinities: 0.5, 4–7, 16

and[ 22 at the hydrolittoral

(H) and littoral (L).

Ordination derived from

Bray–Curtis measures based

on square-root transformed

abundance data for each

subsample per sampling

location. Location labels are

in accordance with Fig. 1

Hydrobiologia (2016) 765:297–315 311

123

diversity increases, the effect of rock size could be less

important as a factor in determining the frequency of

occurrence of encrusting species. Higher diversity and

the presence of marine intertidal specialists lead to an

increased probability of occurrence of encrusting

species, even in the dynamic hydrolittoral zone.

In summary, the results of this study indicate that

local variability due to periodic or stochastic distur-

bances can be significant in shaping faunal commu-

nities encrusting rock surfaces in the hydrolittoral

zone. As salinity increases along the Baltic coast, an

increased heterogeneity of assemblages is evident in

terms of species richness, abundance and diversity.

Multivariate analysis allowed us to distinguish the

patterns found in the hydrolittoral zone from those

observed in shallow littoral assemblages. The low

salinity level observed in the major part of the Baltic

Sea system hinders the formation of the types of

marine assemblages observed in the higher salinity

North Sea region. The structures of hydrolittoral

Fig. 6 Frequency (mean values ± standard error) of encrusting fauna occurrence by given rock size classes in the hydrolittoral

(marked as 0 m) and littoral (3 m). Location labels are in accordance with Fig. 1

312 Hydrobiologia (2016) 765:297–315

123

encrusting assemblages within the Baltic Sea differ in

terms of their dominant species but seem to be derived

from a common species pool with the nearby littoral

communities.

Acknowledgements We would like to thank Tadeusz Stryjek,

Jarek Dobroszek, Karol Wegrzynowski, Mariusz

Wegrzynowski and Kasia Grzelak for their help with the

collection of samples. We would also like to thank Anna

Iglikowska for her help with the multivariate analysis, and the

two anonymous referees for comments leading to an improved

manuscript. The study has been completed, thanks to the

financial support from the National Science Centre to MG

(2011/01/N/ST10/06524) and to PK (2011/03/B/NZ8/02872).

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